Genes & Genomics

, Volume 37, Issue 1, pp 87–95 | Cite as

TE composition of human long noncoding RNAs and their expression patterns in human tissues

  • Donghee Kang
  • Yun-Ji Kim
  • Kwonho Hong
  • Kyudong HanEmail author
Research Article


High-throughput sequencing analyses have revealed that transposable elements (TEs) comprise approximately half of the human genome and frequently involved in genomic rearrangements and instability by various mechanisms. Interestingly, many noncoding RNAs (ncRNAs) contain TEs and the TE-containing ncRNAs that have been implicated in cellular processes and various diseases in mammals. In this study, we retrieved 94 human long noncoding RNAs (lncRNAs; >200 nucleotides in length) from lncRNAdb and analyzed TEs which are embedded within the lncRNAs, focusing on their chromosomal distribution. The result showed that TEs occupy ~27 % of the lncRNA transcripts in mass and lncRNA containing TEs are enriched in human chromosome 11. We further analyzed subfamily of the TEs and found that most of the TEs belong to AluSx and L1 which are the most successful TE subfamilies in the human genome. Numerous lncRNAs have been reported to be expressed in a cell-type specific manner. Thus, using reverse transcription PCR with specific primers for the lncRNAs, we examined their expression pattern in human normal tissues and cancer cells. Most of the lncRNAs were universally amplified from 20 different types of normal human tissues but some of them displayed tissue-specific expression. Especially, 11 lncRNAs were expressed only in human cancer cells, implying the possibility of their involvement in carcinogenesis.


Expression pattern Gene composition Human genome Long noncoding RNAs Transposable elements 



The present work was conducted with funding from the Research Fund of Dankook University in 2013.

Conflict of interest

The authors declare that there is no conflict of interests exists in this paper.

Supplementary material

13258_2014_232_MOESM1_ESM.pdf (77 kb)
Supplementary material 1 (PDF 77 kb)
13258_2014_232_MOESM2_ESM.pdf (33 kb)
Supplementary material 2 (PDF 32 kb)


  1. Alfano G, Vitiello C, Caccioppoli C, Caramico T, Carola A, Szego MJ, McInnes RR, Auricchio A, Banfi S (2005) Natural antisense transcripts associated with genes involved in eye development. Hum Mol Genet 14:913-923Google Scholar
  2. Amaral PP, Mattick JS (2008) Noncoding RNA in development. Mamm Genome 19:454–492Google Scholar
  3. Amaral PP, Clark MB, Gascoigne DK, Dinger ME, Mattick JS (2011) lncRNAdb: a reference database for long noncoding RNAs. Nucleic Acids Res 39:D146–D151PubMedCentralCrossRefPubMedGoogle Scholar
  4. Askarian-Amiri ME, Crawford J, French JD, Smart CE, Smith MA, Clark MB, Ru K, Mercer TR, Thompson ER, Lakhani SR et al (2011) SNORD-host RNA Zfas1 is a regulator of mammary development and a potential marker for breast cancer. RNA 17:878–891Google Scholar
  5. Batzer MA, Deininger PL (2002) Alu repeats and human genomic diversity. Nat Rev Genet 3:370–379CrossRefPubMedGoogle Scholar
  6. Brosnan CA, Voinnet O (2009) The long and the short of noncoding RNAs. Curr Opin Cell Biol 21:416–425CrossRefPubMedGoogle Scholar
  7. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C et al (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491:454–457CrossRefPubMedGoogle Scholar
  8. Cartault F, Munier P, Benko E, Desguerre I, Hanein S, Boddaert N, Bandiera S, Vellayoudom J, Krejbich-Trotot P, Bintner M et al (2012) Mutation in a primate-conserved retrotransposon reveals a noncoding RNA as a mediator of infantile encephalopathy. Proc Natl Acad Sci USA 109:4980–4985PubMedCentralCrossRefPubMedGoogle Scholar
  9. Consortium EP, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET et al (2007) Identification and analysis of functional elements in 1 % of the human genome by the ENCODE pilot project. Nature 447:799–816CrossRefGoogle Scholar
  10. Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10:691–703PubMedCentralCrossRefPubMedGoogle Scholar
  11. Delgado André N, De Lucca FL (2008) Non-coding transcript in T cells (NTT): antisense transcript activates PKR and NF-kappaB in human lymphocytes. Blood Cells Mol Dis 40:227–232Google Scholar
  12. Demers C, Chaturvedi CP, Ranish JA, Juban G, Lai P, Morle F, Aebersold R, Dilworth FJ, Groudine M, Brand M (2007) Activator-mediated recruitment of the MLL2 methyltransferase complex to the beta-globin locus. Mol Cell 27:573–584PubMedCentralCrossRefPubMedGoogle Scholar
  13. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG et al (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789PubMedCentralCrossRefPubMedGoogle Scholar
  14. Dinger ME, Pang KC, Mercer TR, Mattick JS (2008) Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol 4:e1000176PubMedCentralCrossRefPubMedGoogle Scholar
  15. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721–726CrossRefPubMedGoogle Scholar
  16. Feng J, Bi C, Clark BS, Mady R, Shah P, Kohtz JD (2006) The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev 20:1470–1484PubMedCentralCrossRefPubMedGoogle Scholar
  17. Fu X, Ravindranath L, Tran N, Petrovics G, Srivastava S (2006) Regulation of apoptosis by a prostate-specific and prostate cancer-associated noncoding gene, PCGEM1. DNA Cell Biol 25:135–141CrossRefPubMedGoogle Scholar
  18. Guenzl PM, Barlow DP (2012) Macro lncRNAs: a new layer of cis-regulatory information in the mammalian genome. RNA Biol 9:731–741CrossRefPubMedGoogle Scholar
  19. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL et al (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071–1076PubMedCentralCrossRefPubMedGoogle Scholar
  20. Hadjiargyrou M, Delihas N (2013) The intertwining of transposable elements and non-coding RNAs. Int J Mol Sci 14:13307–13328PubMedCentralCrossRefPubMedGoogle Scholar
  21. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  22. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S et al (2012) GENCODE: the reference human genome annotation for the ENCODE Project. Genome Res 22:1760–1774PubMedCentralCrossRefPubMedGoogle Scholar
  23. He H, Nagy R, Liyanarachchi S, Jiao H, Li W, Suster S, Kere J, de la Chapelle A (2009) A susceptibility locus for papillary thyroid carcinoma on chromosome 8q24. Cancer Res 69:625–631PubMedCentralCrossRefPubMedGoogle Scholar
  24. Hernandez A, Garcia B, Obregon MJ (2007) Gene expression from the imprinted Dio3 locus is associated with cell proliferation of cultured brown adipocytes. Endocrinology 148:3968–3976Google Scholar
  25. Johnsson P, Ackley A, Vidarsdottir L, Lui WO, Corcoran M, Grander D, Morris KV (2013) A pseudogene long-noncoding-RNA network regulates PTEN transcription and translation in human cells. Nat Struct Mol Biol 20:440–446PubMedCentralCrossRefPubMedGoogle Scholar
  26. Kelley D, Rinn J (2012) Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 13:R107PubMedCentralCrossRefPubMedGoogle Scholar
  27. Kornienko AE, Guenzl PM, Barlow DP, Pauler FM (2013) Gene regulation by the act of long non-coding RNA transcription. BMC Biol 11:59PubMedCentralCrossRefPubMedGoogle Scholar
  28. Liu AY, Torchia BS, Migeon BR, Siliciano RF (1997) The human NTT gene: identification of a novel 17-kb noncoding nuclear RNA expressed in activated CD4+ T cells. Genomics 39:171–184Google Scholar
  29. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S et al (2010) Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42:1113–1117Google Scholar
  30. Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S (2008) Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics 92:18–25CrossRefPubMedGoogle Scholar
  31. Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595–605CrossRefPubMedGoogle Scholar
  32. Macian F (2005) NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol 5:472–484CrossRefPubMedGoogle Scholar
  33. Mancini-Dinardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM (2006) Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 20:1268–1282PubMedCentralCrossRefPubMedGoogle Scholar
  34. McPherson A, Hormozdiari F, Zayed A, Giuliany R, Ha G, Sun MG, Griffith M, Heravi Moussavi A, Senz J, Melnyk N et al (2011) deFuse: an algorithm for gene fusion discovery in tumor RNA-Seq data. PLoS Comput Biol 7:e1001138PubMedCentralCrossRefPubMedGoogle Scholar
  35. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 105:716–721PubMedCentralCrossRefPubMedGoogle Scholar
  36. Mizuuchi K (1992) Transpositional recombination: mechanistic insights from studies of mu and other elements. Annu Rev Biochem 61:1011–1051CrossRefPubMedGoogle Scholar
  37. Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F, Williams GT (2009) GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 28:195–208CrossRefPubMedGoogle Scholar
  38. Ng K, Pullirsch D, Leeb M, Wutz A (2007) Xist and the order of silencing. EMBO Rep 8:34–39PubMedCentralCrossRefPubMedGoogle Scholar
  39. Niazi F, Valadkhan S (2012) Computational analysis of functional long noncoding RNAs reveals lack of peptide-coding capacity and parallels with 3′ UTRs. RNA 18:825–843PubMedCentralCrossRefPubMedGoogle Scholar
  40. Ørom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q et al (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143:45–58Google Scholar
  41. Qiao HP, Gao WS, Huo JX, Yang ZS (2013) Long non-coding RNA GAS5 functions as a tumor suppressor in renal cell carcinoma. Asian Pac J Cancer Prev 14:1077–1082CrossRefPubMedGoogle Scholar
  42. Raha D, Wang Z, Moqtaderi Z, Wu L, Zhong G, Gerstein M, Struhl K, Snyder M (2010) Close association of RNA polymerase II and many transcription factors with Pol III genes. Proc Natl Acad Sci USA 107:3639–3644PubMedCentralCrossRefPubMedGoogle Scholar
  43. Sado T, Brockdorff N (2013) Advances in understanding chromosome silencing by the long non-coding RNA Xist. Philos Trans R Soc Lond B 368:20110325CrossRefGoogle Scholar
  44. Sanuki R, Onishi A, Koike C, Muramatsu R, Watanabe S, Muranishi Y, Irie S, Uneo S, Koyasu T, Matsui R et al (2011) miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat Neurosci 14:1125–1134CrossRefPubMedGoogle Scholar
  45. Tsai MC, Spitale RC, Chang HY (2011) Long intergenic noncoding RNAs: new links in cancer progression. Cancer Res 71:3–7PubMedCentralCrossRefPubMedGoogle Scholar
  46. Vandeweyer G, Reyniers E, Wuyts W, Rooms L, Kooy RF (2011) CNV-WebStore: online CNV analysis, storage and interpretation. BMC Bioinformatics 12:4Google Scholar
  47. Walter P, Blobel G (1982) Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature 299:691–698CrossRefPubMedGoogle Scholar
  48. Wang X, Song X, Glass CK, Rosenfeld MG (2011) The long arm of long noncoding RNAs: roles as sensors regulating gene transcriptional programs. Cold Spring Harb Perspect Biol 3:a003756PubMedCentralPubMedGoogle Scholar
  49. Warnefors M, Pereira V, Eyre-Walker A (2010) Transposable elements: insertion pattern and impact on gene expression evolution in hominids. Mol Biol Evol 27:1955–1962CrossRefPubMedGoogle Scholar
  50. Wevrick R, Francke U (1997) An imprinted mouse transcript homologous to the human imprinted in Prader-Willi syndrome (IPW) gene. Hum Mol Genet 6:325–332Google Scholar
  51. Willingham AT, Orth AP, Batalov S, Peters EC, Wen BG, Aza-Blanc P, Hogenesch JB, Schultz PG (2005) A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 309:1570–1573CrossRefPubMedGoogle Scholar
  52. Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23:1494–1504PubMedCentralCrossRefPubMedGoogle Scholar
  53. Yan MD, Hong CC, Lai GM, Cheng AL, Lin YW, Chuang SE (2005) Identification and characterization of a novel gene Saf transcribed from the opposite strand of Fas. Hum Mol Genet 14:1465–1474Google Scholar
  54. Zhang A, Zhou N, Huang J, Liu Q, Fukuda K, Ma D, Lu Z, Bai C, Watabe K, Mo YY (2013) The human long non-coding RNA-RoR is a p53 repressor in response to DNA damage. Cell Res 23:340–350PubMedCentralCrossRefPubMedGoogle Scholar
  55. Zhou Y, Zhong Y, Wang Y, Zhang X, Batista DL, Gejman R, Ansell PJ, Zhao J, Weng C, Klibanski A (2007) Activation of p53 by MEG3 non-coding RNA. J Biol Chem 282:24731–24742CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer-Science and Media 2014

Authors and Affiliations

  • Donghee Kang
    • 1
  • Yun-Ji Kim
    • 1
    • 2
  • Kwonho Hong
    • 1
  • Kyudong Han
    • 1
    • 2
    Email author
  1. 1.Department of Nanobiomedical Science & BK21 PLUS NBM Global Research Center for Regenerative MedicineDankook UniversityCheonanRepublic of Korea
  2. 2.DKU-Theragen Institute for NGS Analysis (DTiNa)CheonanRepublic of Korea

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